Abstract
This study focuses on variation in reproductive systems in Acer (maple) species, and how Acer might be a useful genus for understanding floral morphology and the evolution of these highly variable systems. The goals were (1) to conduct a survey of reproductive characters in the genus Acer with an emphasis on floral morphometrics of A. ginnala Maxim., A. tataricum L., and the hybrid A. ginnala × tataricum and (2) present a compilation of the reproductive biology of Acer based on the literature and online information. Morphometric analyses showed that the hybrid A. ginnala × tataricum exhibits intermediacy in vegetative morphology and some floral traits compared to the parents. Literature and an online survey revealed some information on the reproductive biology of 40 Acer species, plus the hybrid, representing only 32.3% of the taxonomic diversity. The reproductive modes of Acer include monoecy, dioecy, trioecy, andromonoecy, androdioecy, and andropolygamy, with a trend towards unisexuality. Temporal patterns of maturation of reproductive parts revealed duodichogamy, heterodichogamy, simultaneous, and dichogamy. The pollination syndrome is entomophilous, anemophilous, and ambophilous. We conclude that the evolutionary and geographic success of Acer lie in the versatility of sexual systems, diverse modes of maturation of reproductive organs, reproductive success, and the ability to colonise wider areas.
Similar content being viewed by others
References
Acevedo-Rodríguez P, Van Welzen PC, Adema F, Van Der Ham RWJM (2011) Sapindaceae. In: Kubitzki K (ed) The families and genera of vascular plants: vascular plants, eudicots (Sapindales, Cucurbitales, Myrtaceae), vol 10. Springer, Berlin, pp 357–407
Barrett SCH, Harder LD (2017) The ecology of mating and its evolutionary consequences in seed plants. Annu Rev Ecol Evol S 48:135–157. https://doi.org/10.1146/annurev-ecolsys-110316-023021
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bawa KS, Beach JH (1981) Evolution of sexual systems in flowering plants. Ann Missouri Bot Gard 68:254–274. https://doi.org/10.2307/2398798
Buerki S, Forest F, Acevedo-Rodríguez P, Callmander MW, Nylader JA, Harrington M, Sanmartín I, Küpfer P, Alvarez N (2009) Plastid and nuclear DNA markers reveal intricate relationships at subfamilial and tribal levels in the soapberry family (Sapindaceae). Mol Phylogenet Evol 51:238–258. https://doi.org/10.1016/j.ympev.2009.01.012
Buerki S, Lowry PP II, Alvarez N, Razafimandimbison SG, Küpfer P, Callmander MW (2010) Phylogeny and circumscription of Sapindaceae revisited: molecular sequence data, morphology and biogeography support recognition of a new family, Xanthoceraceae. Plant Ecol Evol 143:148–159. https://doi.org/10.5091/plecevo.2010.437
Carvalho AMC (2009) Guia de abelhas e outros visitantes de Matayba guianensis (Sapindaceae) em vegetação de Cerrado. Ph.D. thesis, Universidade Federal de Uberlândia, Minas Gerais
Charlesworth D (2012) Theories of the evolution of dioecy. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer, Berlin, pp 33–60
Cronquist A (1981) An integrated system of classification of flowering plants. Columbia University Press, New York
Cronquist A (1988) The evolution and classification of flowering plants, 2nd edn. New York Botanic Gardens, New York
Culley TM, Weller SG, Sakai AK (2002) The evolution of wind pollination in angiosperms. Trends Ecol Evol 17:361–369. https://doi.org/10.1016/S0169-5347(02)02540-5
Dafni A, Kevan PG, Husband BC (2005) Practical pollination biology. In: Dafni A, Kevan PG, Husband BC (eds), Enviroquest Ltd., Cambridge
De Jong PC (1976) Flowering and sex expression in Acer L.: a biosystematics study. H Veenman and Zonen BV, Wageningen
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2017) InfoStat Group. Facultad de Ciencias Agropecuarias, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar
Friedman J, Barrett SCH (2008) A phylogenetic analysis of the evolution of wind pollination in the angiosperms. Int J Plant Sci 169:49–58. https://doi.org/10.1086/523365
Gabriel WJ (1968) Dichogamy in Acer saccharum. Bot Gaz 129:334–338. https://doi.org/10.1086/336453
Gleiser G, Verdú M (2005) Repeated evolution of dioecy from androdioecy in Acer. New Phytol 165:633–640. https://doi.org/10.1111/j.1469-8137.2004.01242.x
Gleiser G, Verdú M, Segarra-Moragues JG, González-Martínez SC, Pannell JR (2008) Disassortative mating, sexual specialization, and the evolution of gender dimorphism in heterodichogamous Acer opalus. Evolution 62:1676–1688. https://doi.org/10.1111/j.1558-5646.2008.00394.x
Gostin I, Minea B (2007) Floral morphogenesis of some species of the Acer genus. An Stiint Univ Al I Cuza 53:52–59
Gutiérrez-Flores C, García-De León FJ, León de la Luz JL, Cota-Sánchez JH (2016) Microsatellite genetic diversity and mating systems in the columnar cactus Pachycereus pringlei (Cactaceae). Perspect Plant Ecol 22:1–10. https://doi.org/10.1016/j.ppees.2016.06.003
Gutiérrez-Flores C, Cota-Sánchez JH, León-de la Luz JL, García-De León FJ (2017) Disparity in floral traits and breeding systems in the iconic columnar cactus Pachycereus pringlei (Cactaceae). Flora 235:18–28. https://doi.org/10.1016/j.flora.2017.08.007
Gutiérrez-Flores C, León de la Luz JL, García-De León FJ, Cota-Sánchez JH (2018) Variation in chromosome number and breeding systems: implications for diversification in Pachycereus pringlei (Cactaceae). Comp Cytogen 12:61–82. https://doi.org/10.3897/CompCytogen.v12i1.21554
Hall BA (1951) The floral anatomy of the genus Acer. Am J Bot 38:793–799. https://doi.org/10.2307/2438204
Haragsim O (1977) The nectar secretion of maple (Acer platanoides L.) and sycamore (A. pseudoplatanus L.). Apidologie 8:363–368. https://doi.org/10.1051/apido:19770407
Harrington MG, Edwards KJ, Johnson SA, Chase MW, Gadek PA (2005) Phylogenetic inference in Sapindaceae sensu lato using plastid matK and rbcL DNA sequences. Syst Bot 36:366–382. https://doi.org/10.1600/0363644054223549
Harrington MG, Biffin E, Gadek PA (2009) Comparative study of the evolution of nuclear ribosomal spacers incorporating secondary structure analyzes within Dodonaeoideae, Hippocastanoideae and Xanthoceroideae (Sapindaceae). Mol Phylogenet Evol 50:364–375. https://doi.org/10.1016/j.ympev.2008.11.010
Hesse H (1979) Ultrastruktur und verteilungs des pollenkitts in der insekten und windblütigen gattung Acer (Aceraceae). Plant Syst Evol 131:277–289. https://doi.org/10.1007/BF00984259
Hibbs DE, Fischer BC (1979) Sexual and vegetative reproduction of striped maple (Acer pensylvanicum L.). Bull Torrey Bot Club 106:222–227. https://doi.org/10.2307/2484558
Hickey M, King C (1988) 100 families of flowering plants, 2nd edn. Cambridge University Press, Cambridge
Iddrisu MN, Ritland K (2004) Genetic variation, population structure, and mating system in big leaf maple (Acer macrophyllum Pursh). Can J Bot 82:1817–1825. https://doi.org/10.1139/B04-136
Jacobson AL (1996) North America landscape trees. Ten Speed Press, Berkeley
Jones EW (1945) Acer L. J Ecol 32:215–219. https://doi.org/10.2307/2256711
Justice DEC (1995) The systematics of Rocky Mountain Maple, Acer glabrum Torrey. M.Sc. Thesis, University of British Columbia, British Columbia
Lenza E, Ferreira JN (2000) Biologia floral de Serjania erecta Radlk. (Sapindaceae): um caso de dioicia temporal. Boletim do Herbário Ezechias Paulo Heringer 6:23–37
Li J, Yue J, Shoup S (2006) Phylogenetics of Acer (Aceroideae, Sapindaceae) based on nucleotide sequences of two chloroplast non-coding regions. Harv Pap Bot 11:101–115. https://doi.org/10.3100/1043-4534(2006)11%5B101:POAASB%5D2.0.CO;2
Lima HA, Somner GV, Giulietti AM (2016) Duodichogamy and sex lability in Sapindaceae: the case of Paullinia weinmanniifolia. Plant Syst Evol 302:109–120. https://doi.org/10.1007/s00606-015-1247-5
Lloyd DG (1980) Sexual strategies in plants. New Phytol 86:69–79. https://doi.org/10.1111/j.1469-8137.1980.tb00780.x
Luo S, Zhang D, Renner SS (2007) Duodichogamy and androdioecy in the Chinese Phyllanthaceae Bridelia tomentosa. Am J Bot 94:260–265. https://doi.org/10.3732/ajb.94.2.260
Luo YB, Yu JL, Tong ZK, Zhao HB (2017) Flower development of different genders in the morphologically andromonoecious but functionally monoecious plant Acer elegantulum Fang et P.L. Chiu. Flora 233:179–185. https://doi.org/10.1016/j.flora.2017.06.006
Maeglin RR, Ohmann LF (1973) Boxelder (Acer negundo): a review and commentary. Bull Torrey Bot Club 100:357–363. https://doi.org/10.2307/2484104
Matsui K (1991) Pollination ecology of four Acer species in Japan with special reference to bee pollinators. Plant Species Biol 6:117–120. https://doi.org/10.1111/j.1442-1984.1991.tb00218.x
Matsui K (1995) Sex expression, sex change and fruiting habit in an Acer rufinerve population. Ecol Res 10:65–74. https://doi.org/10.1007/BF02347656
Meehan T (1868) Sexual law in Acer dasycarpum Ehrb. Proc Acad Nat Sci Philadelphia 20:140–141
Nanami S, Kawaguchi H, Yamakura T (2004) Sex change towards female in dying Acer rufinerve trees. Ann Bot 93:733–740. https://doi.org/10.1093/aob/mch093
Peck CJ, Lersten NR (1991) Papillate stigmas in Acer (Aceraceae). Bull Torrey Bot Club 118:20–23. https://doi.org/10.2307/2996971
Primack RB, McCall C (1986) Gender variation in a red maple population (Acer rubrum; Aceraceae): a seven-year study of a “polygamodioecious” species. Am J Bot 73:1239–1248. https://doi.org/10.2307/2444057
R Core Team (2017) R: a language and environment for statistical computing. R Found. Stat. Comput. Vienna, Austria. https://www.r-project.org/
Renner SS (2014) The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am J Bot 101:1588–1596. https://doi.org/10.3732/ajb.1400196
Renner SS, Ricklefs RE (2005) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606. https://doi.org/10.2307/2445418
Renner SS, Beenken L, Grimm GW, Kocyan A, Ricklefs RE (2007) The evolution of dioecy, heterodichogamy, and labile sex expression in Acer. Evolution 61:2701–2719. https://doi.org/10.1111/j.1558-5646.2007.00221.x
Richards AJ (1986) Plant breeding systems. George Allen and Unwin, London
Rosado A (2017) Spindaceae sensu stricto no Estado do Paraná. Ph.D. Thesis, Universidade Estadual de Maringá, Paraná
Sato T (2002) Phenology of sex expression and gender variation in a heterodichogamous maple, Acer japonicum. Ecology 83:1226–1238. https://doi.org/10.1890/00129658(2002)083%5B1226:POSEAG%5D2.0.CO;2
Shang H, Luo YB, Bai WN (2012) Influence of asymmetrical mating patterns and male reproductive success on the maintenance of sexual polymorphism in Acer pictum subsp. mono (Aceraceae). Mol Ecol 21:3869–3878. https://doi.org/10.1111/j.1365-294X.2012.05555.x
Soza VL, Brunet J, Liston A, Salles-Smith P, Di Stilio VS (2012) Phylogenetic insights into the correlates of dioecy in meadowrues (Thalictrum, Ranunculaceae). Mol Phylogenet Evol 63:180–192. https://doi.org/10.1016/j.ympev.2012.01.009
Spichiger RE, Savolainen V, Figeat M, Jeanmonod D (2004) Systematic botany of flowering plants: a new phylogenetic approach to angiosperms of the temperate and tropical regions. Science Publishers, Enfield
Sullivan JR (1983) Comparative reproductive biology of Acer pensylvanicum and A. spicatum (Aceraceae). Am J Bot 70:916–924. https://doi.org/10.2307/2442945
Tal O (2009) Acer pseudoplatanus (Sapindaceae): heterodichogamy and thrips pollination. Plant Syst Evol 278:211–221. https://doi.org/10.1007/s00606-008-0141-9
Tamura S, Kudo G (2000) Wind pollination and insect pollination of two temperate willow species, Salix miyabeana and Salix sachalinensis. Plant Ecol 147:185–192. https://doi.org/10.1023/A:10098705
Tingzhi X, Yousheng C, De Jong PC, Oterdoom HJ, Chang CS (2008) Aceraceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol. 11 (Oxalidaceae through Aceraceae). Missouri Botanical Garden Press, St. Louis. http://flora.huh.harvard.edu/China/mss/volume11/Aceraceae.pdf. Accessed June 2017
Tripic R (2010) Contribution to the knowledge of the flowering phenology and sex expression in Acer tataricum L. from Montenegro. Nat Montenegr 9:183–193
Van Gelderen CJ, Van Gelderen DM (1999) Maples for gardens: a color encyclopedia. Timber Press, Portland
Van Gelderen DM, De Jong PC, Oterdoom HJ (1994) Maples of the world. Timber Press, Portland
Weryszko-Chimielewska E, Sulborska A (2011) Morphological characters of the flowers and the structure of the nectaries of Acer platanoides L. Acta Agrobot 64:19–28. https://doi.org/10.5586/aa.2011.026
Whitehead DR (1969) Wind pollination in the angiosperms: evolutionary and environmental considerations. Evolution 23:28–35. https://doi.org/10.2307/2406479
Whitehead DR (1983) Wind pollination: some ecological and evolutionary perspectives. In: Real L (ed) Pollination biology. Academic Press, Orlando, pp 97–108
Yadav N, Padey AK, Bhatnagar AK (2016) Cryptic monoecy and floral morph types in Acer oblongum (Sapindaceae): an endangered taxon. Flora 224:183–190. https://doi.org/10.1016/j.flora.2016.07.018
Yang ZQ, Zhang DY, Bai WN (2015) The functional significance of a stigma color polymorphism in Acer pictum subsp. mono (Aceraceae). J Plant Ecol 8:166–172. https://doi.org/10.1093/jpe/rtv018
You-Sheng C (2007) Two newly recorded species of Acer (Aceraceae) in China. Acta Phytotax Sin 45:337–340. https://doi.org/10.1360/aps050172
Zhang L, Shang H, Luo Y, Cheng X, Weining B (2011) Morphology and cytology of three flower phenotypes in a duodichogamous tree species, Acer mono. Biodiversity Science 19:551–557. https://doi.org/10.3724/SP.J.1003.2011.07035
Acknowledgements
We thank Dr. Carlos E.P. Nunes and two anonymous reviewers for their valuable feedback to improve the manuscript. We thank the Government of Canada and the Emerging Leaders of the Americas Program (ELAP) for awarding a scholarship to A. Rosado. We are indebted to Peter Stevens, Dewey Litwiller, and personnel of the Cota-Sánchez’ Plant Systematics Laboratory (C. Gutiérrez-Flores and D. Falconer) for their insights, critical comments, and proof reading of early drafts of the manuscript. M. Mierau and G. Liu provided technical support. We also express our gratitude to the curators of DAO and SASK for providing herbarium material for investigation. This research was partially supported by funding from the Flora of Saskatchewan Association and the University of Saskatchewan Bridge Fund to JHCS.
Author information
Authors and Affiliations
Contributions
A.R. conducted fieldwork, gathered and analysed macro- and micromorphological data and contributed to analyses, writing, and discussion of manuscript. R.V.V. assisted in fieldwork, conducted statistical analyses, and contributed to writing and discussion of manuscript. J.H.C.S. provided research funds, supervised the investigation, conducted fieldwork, gathered data, and led the structure, writing, and discussion of manuscript.
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
40415_2018_452_MOESM2_ESM.docx
Summary of results of the Generalised Linear Mixed Model (GLMM) using Poisson distribution and Log link function to analyse the number of flowers per Acer species and the GLMM using Normal distribution and Identity link function to analyse flower diameter, flower height, stamen height, and stigma height (only for hermaphrodite flowers) in the Acer species (DOCX 104 kb)
Rights and permissions
About this article
Cite this article
Rosado, A., Vera-Vélez, R. & Cota-Sánchez, J.H. Floral morphology and reproductive biology in selected maple (Acer L.) species (Sapindaceae). Braz. J. Bot 41, 361–374 (2018). https://doi.org/10.1007/s40415-018-0452-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-018-0452-1